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Filopodial-Tension Model of Convergent-Extension of Tissues

In convergent-extension (CE), a planar-polarized epithelial tissue elongates (extends) in-plane in one direction while shortening (converging) in the perpendicular in-plane direction, with the cells both elongating and intercalating along the converging axis. CE occurs during the development of most...

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Autores principales: Belmonte, Julio M., Swat, Maciej H., Glazier, James A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4913901/
https://www.ncbi.nlm.nih.gov/pubmed/27322528
http://dx.doi.org/10.1371/journal.pcbi.1004952
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author Belmonte, Julio M.
Swat, Maciej H.
Glazier, James A.
author_facet Belmonte, Julio M.
Swat, Maciej H.
Glazier, James A.
author_sort Belmonte, Julio M.
collection PubMed
description In convergent-extension (CE), a planar-polarized epithelial tissue elongates (extends) in-plane in one direction while shortening (converging) in the perpendicular in-plane direction, with the cells both elongating and intercalating along the converging axis. CE occurs during the development of most multicellular organisms. Current CE models assume cell or tissue asymmetry, but neglect the preferential filopodial activity along the convergent axis observed in many tissues. We propose a cell-based CE model based on asymmetric filopodial tension forces between cells and investigate how cell-level filopodial interactions drive tissue-level CE. The final tissue geometry depends on the balance between external rounding forces and cell-intercalation traction. Filopodial-tension CE is robust to relatively high levels of planar cell polarity misalignment and to the presence of non-active cells. Addition of a simple mechanical feedback between cells fully rescues and even improves CE of tissues with high levels of polarity misalignments. Our model extends easily to three dimensions, with either one converging and two extending axes, or two converging and one extending axes, producing distinct tissue morphologies, as observed in vivo.
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spelling pubmed-49139012016-07-06 Filopodial-Tension Model of Convergent-Extension of Tissues Belmonte, Julio M. Swat, Maciej H. Glazier, James A. PLoS Comput Biol Research Article In convergent-extension (CE), a planar-polarized epithelial tissue elongates (extends) in-plane in one direction while shortening (converging) in the perpendicular in-plane direction, with the cells both elongating and intercalating along the converging axis. CE occurs during the development of most multicellular organisms. Current CE models assume cell or tissue asymmetry, but neglect the preferential filopodial activity along the convergent axis observed in many tissues. We propose a cell-based CE model based on asymmetric filopodial tension forces between cells and investigate how cell-level filopodial interactions drive tissue-level CE. The final tissue geometry depends on the balance between external rounding forces and cell-intercalation traction. Filopodial-tension CE is robust to relatively high levels of planar cell polarity misalignment and to the presence of non-active cells. Addition of a simple mechanical feedback between cells fully rescues and even improves CE of tissues with high levels of polarity misalignments. Our model extends easily to three dimensions, with either one converging and two extending axes, or two converging and one extending axes, producing distinct tissue morphologies, as observed in vivo. Public Library of Science 2016-06-20 /pmc/articles/PMC4913901/ /pubmed/27322528 http://dx.doi.org/10.1371/journal.pcbi.1004952 Text en © 2016 Belmonte et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Belmonte, Julio M.
Swat, Maciej H.
Glazier, James A.
Filopodial-Tension Model of Convergent-Extension of Tissues
title Filopodial-Tension Model of Convergent-Extension of Tissues
title_full Filopodial-Tension Model of Convergent-Extension of Tissues
title_fullStr Filopodial-Tension Model of Convergent-Extension of Tissues
title_full_unstemmed Filopodial-Tension Model of Convergent-Extension of Tissues
title_short Filopodial-Tension Model of Convergent-Extension of Tissues
title_sort filopodial-tension model of convergent-extension of tissues
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4913901/
https://www.ncbi.nlm.nih.gov/pubmed/27322528
http://dx.doi.org/10.1371/journal.pcbi.1004952
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